Culling-induced social perturbation in Eurasian badgers Meles meles and the management of TB in cattle: an analysis of a critical problem in applied ecology

The Eurasian badger (Meles meles) is implicated in the transmission of bovine tuberculosis (TB) to cattle in the UK and Republic of Ireland. Badger culling has been employed for the control of TB in cattle in both countries, with varying results. Social perturbation of badger populations following culling has been proposed as an explanation for the failure of culling to consistently demonstrate significant reductions in cattle TB. Field studies indicate that culling badgers may result in increased immigration into culled areas, disruption of territoriality, increased ranging and mixing between social groups. Our analysis shows that some measures of sociality may remain significantly disrupted for up to 8 years after culling. This may have epidemiological consequences because previous research has shown that even in a relatively undisturbed badger population, movements between groups are associated with increases in the incidence of Mycobacterium bovis infection. This is consistent with the results from a large-scale field trial, which demonstrated decreased benefits of culling at the edges of culled areas, and an increase in herd breakdown rates in neighbouring cattle.     

Effects of culling on badger abundance: implications for tuberculosis control

Culling is often considered as a tool for controlling wildlife diseases that can also infect people or livestock. Culling European badgers Meles meles can cause both positive and negative effects on the incidence of bovine tuberculosis (TB) in cattle. One factor likely to influence the outcome of different badger-culling strategies for cattle TB is the reduction in badger population density achieved. However, this reduction is difficult to measure because badgers, being nocturnal and fossorial, are difficult to count. Here, we use indices of badger abundance to measure the population impacts of two culling strategies tested in Britain. The densities of badger setts and latrines recorded before culling were correlated with the densities of badgers captured on initial culls, suggesting that both were indices of actual badger abundance. Widespread 'proactive' culling was associated with a 73% reduction in the density of badger latrines, a 69% reduction in the density of active burrows and a 73% reduction in the density of road-killed badgers. This population reduction was achieved by a coordinated effort entailing widespread and repeated trapping over several years. However, this strategy caused only modest reductions in cattle TB incidence in culled areas and elevated incidence in neighbouring unculled areas. Localized 'reactive' culling caused a 26% reduction in latrine density, a 32% reduction in active burrow density and a 10% reduction in the density of road-killed badgers, but apparently increased the incidence of cattle TB. These results indicate that the relationship between badger population reduction and TB transmission to cattle is strongly non-linear, probably because culling prompts changes in badger behaviour that influence transmission rates. These findings raise serious questions about the capacity of badger culling to contribute to the control of cattle TB in Britain.     

Culling-induced changes in badger (Meles meles) behaviour, social organisation and the epidemiology of bovine tuberculosis

In the UK, attempts since the 1970s to control the incidence of bovine tuberculosis (bTB) in cattle by culling a wildlife host, the European badger (Meles meles), have produced equivocal results. Culling-induced social perturbation of badger populations may lead to unexpected outcomes. We test predictions from the 'perturbation hypothesis', determining the impact of culling operations on badger populations, movement of surviving individuals and the influence on the epidemiology of bTB in badgers using data dervied from two study areas within the UK Government's Randomised Badger Culling Trial (RBCT). Culling operations did not remove all individuals from setts, with between 34-43% of badgers removed from targeted social groups. After culling, bTB prevalence increased in badger social groups neighbouring removals, particularly amongst cubs. Seventy individual adult badgers were fitted with radio-collars, yielding 8,311 locational fixes from both sites between November 2001 and December 2003. Home range areas of animals surviving within removed groups increased by 43.5% in response to culling. Overlap between summer ranges of individuals from Neighbouring social groups in the treatment population increased by 73.3% in response to culling. The movement rate of individuals between social groups was low, but increased after culling, in Removed and Neighbouring social groups. Increased bTB prevalence in Neighbouring groups was associated with badger movements both into and out of these groups, although none of the moving individuals themselves tested positive for bTB. Significant increases in both the frequency of individual badger movements between groups and the emergence of bTB were observed in response to culling. However, no direct evidence was found to link the two phenomena. We hypothesise that the social disruption caused by culling may not only increase direct contact and thus disease transmission between surviving badgers, but may also increase social stress within the surviving population, causing immunosuppression and enhancing the expression of disease.     

Perturbing implications of wildlife ecology for disease control

Britain's Randomised Badger Culling Trial provides robust evidence of the role badgers have in transmission of Mycobacterium bovis to cattle. Culling badgers perturbed their social structure, and brought positive and negative effects for bovine tuberculosis incidence in cattle, leading to the conclusion that culling could not make a meaningful contribution to disease control. The RBCT highlights the complexities of disease transmission in social animals and the importance of host ecology for controlling wildlife diseases.     

Spatial Targeting for Bovine Tuberculosis Control: Can the Locations of Infected Cattle Be Used to Find Infected Badgers?

Bovine tuberculosis is a disease of historical importance to human health in the UK that remains a major animal health and economic issue. Control of the disease in cattle is complicated by the presence of a reservoir species, the Eurasian badger. In spite of uncertainty in the degree to which cattle disease results from transmission from badgers, and opposition from environmental groups, culling of badgers has been licenced in two large areas in England. Methods to limit culls to smaller areas that target badgers infected with TB whilst minimising the number of uninfected badgers culled is therefore of considerable interest. Here, we use historical data from a large-scale field trial of badger culling to assess two alternative hypothetical methods of targeting TB-infected badgers based on the distribution of cattle TB incidents: (i) a simple circular ‘ring cull’; and (ii) geographic profiling, a novel technique for spatial targeting of infectious disease control that predicts the locations of sources of infection based on the distribution of linked cases. Our results showed that both methods required coverage of very large areas to ensure a substantial proportion of infected badgers were removed, and would result in many uninfected badgers being culled. Geographic profiling, which accounts for clustering of infections in badger and cattle populations, produced a small but non-significant increase in the proportion of setts with TB-infected compared to uninfected badgers included in a cull. It also provided no overall improvement at targeting setts with infected badgers compared to the ring cull. Cattle TB incidents in this study were therefore insufficiently clustered around TB-infected badger setts to design an efficient spatially targeted cull; and this analysis provided no evidence to support a move towards spatially targeted badger culling policies for bovine TB control.     

The Duration of the Effects of Repeated Widespread Badger Culling on Cattle Tuberculosis Following the Cessation of Culling

Background

In the British Isles, control of cattle tuberculosis (TB) is hindered by persistent infection of wild badger (Meles meles) populations. A large-scale field trial—the Randomised Badger Culling Trial (RBCT)—previously showed that widespread badger culling produced modest reductions in cattle TB incidence during culling, which were offset by elevated TB risks for cattle on adjoining lands. Once culling was halted, beneficial effects inside culling areas increased, while detrimental effects on adjoining lands disappeared. However, a full assessment of the utility of badger culling requires information on the duration of culling effects.

Methodology/Principal Findings

We monitored cattle TB incidence in and around RBCT areas after culling ended. We found that benefits inside culled areas declined over time, and were no longer detectable by three years post-culling. On adjoining lands, a trend suggesting beneficial effects immediately after the end of culling was insignificant, and disappeared after 18 months post-culling. From completion of the first cull to the loss of detectable effects (an average five-year culling period plus 2.5 years post-culling), cattle TB incidence was 28.7% lower (95% confidence interval [CI] 20.7 to 35.8% lower) inside ten 100 km² culled areas than inside ten matched no-culling areas, and comparable (11.7% higher, 95% CI: 13.0% lower to 43.4% higher, p  =  0.39) on lands ≤2 km outside culled and no-culling areas. The financial costs of culling an idealized 150 km² area would exceed the savings achieved through reduced cattle TB, by factors of 2 to 3.5.

Conclusions/Significance

Our findings show that the reductions in cattle TB incidence achieved by repeated badger culling were not sustained in the long term after culling ended and did not offset the financial costs of culling. These results, combined with evaluation of alternative culling methods, suggest that badger culling is unlikely to contribute effectively to the control of cattle TB in Britain.     

Local cattle and badger populations affect the risk of confirmed tuberculosis in British cattle herds

Background

The control of bovine tuberculosis (bTB) remains a priority on the public health agenda in Great Britain, after launching in 1998 the Randomised Badger Culling Trial (RBCT) to evaluate the effectiveness of badger (Meles meles) culling as a control strategy. Our study complements previous analyses of the RBCT data (focusing on treatment effects) by presenting analyses of herd-level risks factors associated with the probability of a confirmed bTB breakdown in herds within each treatment: repeated widespread proactive culling, localized reactive culling and no culling (survey-only).

Methodology/Principal Findings

New cases of bTB breakdowns were monitored inside the RBCT areas from the end of the first proactive badger cull to one year after the last proactive cull. The risk of a herd bTB breakdown was modeled using logistic regression and proportional hazard models adjusting for local farm-level risk factors. Inside survey-only and reactive areas, increased numbers of active badger setts and cattle herds within 1500 m of a farm were associated with an increased bTB risk. Inside proactive areas, the number of M. bovis positive badgers initially culled within 1500 m of a farm was the strongest predictor of the risk of a confirmed bTB breakdown.

Conclusions/Significance

The use of herd-based models provide insights into how local cattle and badger populations affect the bTB breakdown risks of individual cattle herds in the absence of and in the presence of badger culling. These measures of local bTB risks could be integrated into a risk-based herd testing programme to improve the targeting of interventions aimed at reducing the risks of bTB transmission.     

Localized reactive badger culling increases risk of bovine tuberculosis in nearby cattle herds

Human and livestock diseases can be difficult to control where infection persists in wildlife populations. Control of bovine tuberculosis (bTB) in British cattle is complicated by the maintenance of Mycobacterium bovis (the causative agent of bTB) in badgers, acting as reservoirs of infection. Although over 20 000 badgers were culled to control bTB between 1975 and 1997, the incidence of bTB in cattle has substantially increased in parts of Great Britain in recent decades. Our case-control study, involving 1208 cattle herds, provides further evidence of the detrimental effect of localized reactive badger culling in response to the disclosure of a confirmed bTB herd breakdown in cattle. The presence of any reactive badger culling activity and increased numbers of badgers culled in the vicinity of a herd were associated with significantly increased bTB risk, even after adjusting for other important local risk factors. Such findings may partly explain why some earlier localized approaches to bTB control were ineffective.     

Comparing badger (Meles meles) management strategies for reducing tuberculosis incidence in cattle

Bovine tuberculosis (bTB), caused by Mycobacterium bovis, continues to be a serious economic problem for the British cattle industry. The Eurasian badger (Meles meles) is partly responsible for maintenance of the disease and its transmission to cattle. Previous attempts to manage the disease by culling badgers have been hampered by social perturbation, which in some situations is associated with increases in the cattle herd incidence of bTB. Following the licensing of an injectable vaccine, we consider the relative merits of management strategies to reduce bTB in badgers, and thereby reduce cattle herd incidence. We used an established simulation model of the badger-cattle-TB system and investigated four proposed strategies: business as usual with no badger management, large-scale proactive badger culling, badger vaccination, and culling with a ring of vaccination around it. For ease of comparison with empirical data, model treatments were applied over 150 km(2) and were evaluated over the whole of a 300 km(2) area, comprising the core treatment area and a ring of approximately 2 km. The effects of treatment were evaluated over a 10-year period comprising treatment for five years and the subsequent five year period without treatment. Against a background of existing disease control measures, where 144 cattle herd incidents might be expected over 10 years, badger culling prevented 26 cattle herd incidents while vaccination prevented 16. Culling in the core 150 km(2) plus vaccination in a ring around it prevented about 40 cattle herd breakdowns by partly mitigating the negative effects of culling, although this approach clearly required greater effort. While model outcomes were robust to uncertainty in parameter estimates, the outcomes of culling were sensitive to low rates of land access for culling, low culling efficacy, and the early cessation of a culling strategy, all of which were likely to lead to an overall increase in cattle disease.     

The role of setts in badger (Meles meles) group size, breeding success and status of TB (Mycobacterium bovis)

This paper examines the relationship between the number of occupied setts in a badger social group territory and badger group size, breeding success, and status of infection with Mycobacterium bovis (TB). The data used were from a long-term epidemiological and ecological study of a high-density population of badgers Meles meles in south-west England. The number of occupied setts in a social group was significantly and positively related to the number of badgers caught in the social group, so that as a social group increases in size, badgers occupy more of the available setts. This relationship remained significant when numbers of adults, adult males and adult females were examined. The number of breeding females, number of cubs and sex ratio was not related to the number of occupied setts in a social group. It is possible that the advantages to breeding females of a larger number of setts available to breed in might be outweighed by the increased aggression found in larger groups. The TB score for prevalence and for incidence of social groups was significantly and positively related to the number of occupied setts in a social group, such that the more occupied setts there were in a territory, the higher the TB index of the group. Possibly the setts themselves contribute to the persistence of TB within social groups, or badgers infected with TB might show a difference in behaviour from uninfected badgers resulting in their increased use of outlying setts.     

Herd-level risk factors associated with tuberculosis breakdowns among cattle herds in England before the 2001 foot-and-mouth disease epidemic

A case-control study of the factors associated with the risk of a bovine tuberculosis (TB) breakdown in cattle herds was undertaken within the randomized badger culling trial (RBCT). TB breakdowns occurring prior to the 2001 foot-and-mouth disease epidemic in three RBCT triplets were eligible to be cases; controls were selected from the same RBCT area. Data from 151 case farms and 117 control farms were analysed using logistic regression. The strongest factors associated with an increased TB risk were movement of cattle onto the farm from markets or farm sales, operating a farm over multiple premises and the use of either covered yard or 'other' housing types. Spreading artificial fertilizers or farmyard manure on grazing land were both associated with decreased risk. These first case-control results from the RBCT will be followed by similar analyses as more data become available.     

Social organization and movement influence the incidence of bovine tuberculosis in an undisturbed high-density badger Meles meles population

1. The culling of European badgers Meles meles has been a central part of attempts to control bovine tuberculosis (TB) in British cattle for many years. Recent results, however, indicate that this approach could in practice enhance disease spread. 2. This paper looks at the relationship between TB incidence and badger ecology in a high-density population in south-west England, which has been the subject of a long-term intensive study. The principal aims were to relate the probability of TB incidence, as detected by culture of clinical samples (i.e. excretion of bacilli), at the level of the individual and of the social group to demographic processes, movement, social organization and disease dynamics. 3. The probability of an individual being an incident case was greater in groups where TB was already present, although this was less influential in groups that were subject to some instability in numbers. Both individuals and groups were more likely to be incident cases where the social group was diminishing in size, although no relationship was observed with group size itself. This suggests that the process of group size reduction rather than group size per se has most influence on disease dynamics. The likelihood that either an individual or a group was an incident case was positively correlated with both individual and group-level movement. When the proportion of females in a social group was high, the positive association between movement and incidence was found to be more pronounced and there was a significantly higher probability of incident cases among males. 4. These relationships highlight the importance of social structure in driving TB transmission dynamics in this stable, high-density badger population. The results support the idea that a stable social structure mitigates against new incident cases of disease, and are consistent with the contention that badger culling may create the social circumstances for enhanced transmission of TB.     

Inferring Mycobacterium bovis transmission between cattle and badgers using isolates from the Randomised Badger Culling Trial

Mycobacterium bovis (M. bovis) is a causative agent of bovine tuberculosis, a significant source of morbidity and mortality in the global cattle industry. The Randomised Badger Culling Trial was a field experiment carried out between 1998 and 2005 in the South West of England. As part of this trial, M. bovis isolates were collected from contemporaneous and overlapping populations of badgers and cattle within ten defined trial areas. We combined whole genome sequences from 1,442 isolates with location and cattle movement data, identifying transmission clusters and inferred rates and routes of transmission of M. bovis. Most trial areas contained a single transmission cluster that had been established shortly before sampling, often contemporaneous with the expansion of bovine tuberculosis in the 1980s. The estimated rate of transmission from badger to cattle was approximately two times higher than from cattle to badger, and the rate of within-species transmission considerably exceeded these for both species. We identified long distance transmission events linked to cattle movement, recurrence of herd breakdown by infection within the same transmission clusters and superspreader events driven by cattle but not badgers. Overall, our data suggests that the transmission clusters in different parts of South West England that are still evident today were established by long-distance seeding events involving cattle movement, not by recrudescence from a long-established wildlife reservoir. Clusters are maintained primarily by within-species transmission, with less frequent spill-over both from badger to cattle and cattle to badger.     

Reports on badgers Meles meles in Dutch newspapers 1900–2013: same animals,different framings?

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Weather influences trapping success for tuberculosis management in European badgers (<Emphasis Type="Italic">Meles meles</Emphasis>)

European badgers (Meles meles) in Ireland and the UK are a reservoir for Mycobacterium bovis, the causative agent of bovine tuberculosis (TB). A number of interventions have been evaluated in attempts to control bovine TB within badger populations, and many of which rely on the capture of badgers. One strategy being implemented within Ireland is intramuscular vaccination using Bacillus Calmette-Guérin (BCG), as an alternative to badger culling. The success of vaccination as a disease control strategy depends on the ability to capture badgers and administer vaccines; thus, trapping success is crucial to effectively vaccinate the population (maximize vaccine coverage). A field vaccine trial was conducted in County Kilkenny, Ireland, from 2010–2013. We used data from this trial to evaluate the association between weather (precipitation and temperature data), badger sett characteristics, and badger trapping success. Approximately 10% of capture efforts resulted in a badger capture. Our results indicate that badger captures were the highest in drizzle, rain, and heavy rain weather conditions, and when minimum temperatures ranged from 3–8 °C. Badger captures were the highest at main setts (large burrow systems), and when sett activity scores were high (qualitative classes 4 or 5). Using local precipitation and temperature data in conjunction with observed sett characteristics provides wildlife managers with guidelines to optimize trapping success. Implementing capture operations under optimal conditions should increase the trapping success of badgers and allow for increased delivery of vaccines to manage bovine TB.     

Is Mycobacterium bovis in the environment important for the persistence of bovine tuberculosis?

Mycobacterium bovis is the causative agent of bovine tuberculosis (bTB) in cattle and wildlife. Direct aerosol contact is thought to be the primary route of infection between conspecifics, whereas indirect transmission via an environmental reservoir of M. bovis is generally perceived not to be a significant source for infection. Here, we report on the application of molecular technology (PCR) to quantify the prevalence of M. bovis in the environment and to explore its epidemiological significance. We show that the detectability of viable M. bovis at badger setts and latrines is strongly linked to the frequency of M. bovis excretion by infected badgers, and that putative M. bovis in the environment is prevalent on a large proportion of endemic cattle farms in Britain. These results raise important questions about the role of an environmental reservoir in bTB persistence.     

Environmental risk factors associated with bovine tuberculosis among cattle in high-risk areas

Our research shows that environmental features are important predictors of bovine tuberculosis (bTB) in British cattle herds in high-prevalence regions. Data from 503 case and 808 control farms included in the randomized badger culling trial (RBCT) were analysed. bTB risk increased in larger herds and on farms with greater areas of maize, deciduous woodland and marsh, whereas a higher percentage of boundaries composed of hedgerows decreased the risk. The model was tested on another case–control study outside RBCT areas, and here it had a much smaller predictive power. This suggests that different infection dynamics operate outside high-risk areas, although it is possible that unknown confounding factors may also have played a role.     

Impact of culling on relative abundance of the European badger (Meles meles) in Ireland

The European Badger (Meles meles) has been implicated in the epidemiology of bovine tuberculosis in cattle populations in the Republic of Ireland. Badger populations have been subject to a culling regime in areas with chronic histories of bTB cattle herd breakdowns. Removal data from 2004 to 2010 were used to model the impact of culling on populations in areas under capture. Additionally, changes in field signs of badger activity were used as an index of abundance to support, or otherwise, the outcomes of the removal models. Significant reductions in standardised badger captures over time were found across three large study areas (total area, 1,355 km²). Assuming that all inactive setts were vacant, an overall linear trend model suggested that badger captures had decreased by 78 % for setts with 6 years of repeated capturing operations. Given the uncertainty associated with the relationship between sett activity and badger presence, we repeated the linear modelling using two ‘what if’ scenarios. Assuming that individual badgers were missed on 10 % or 20 % of occasions at inactive setts, the estimated decline over 6 years is lowered to 71 % or 64 %, respectively. The decline profile consisted of a steep initial decrease in captures within the first 2 years, followed by a more gradual decrease thereafter. The number of active openings at setts (burrows) declined significantly in all three areas; but the magnitude of this decline varied significantly amongst study areas (41–82 %). There was a significant increase in the probability of setts becoming dormant with time. The removal programme was more intense (mean, 0.45 badgers culled km^?2 year^?1) than previous experimental badger removals in Ireland but some captures may be attributed to immigrant badgers as no attempt was made to limit inward dispersal from areas not under management. Results from this study suggest that significant reductions in badger density occurred in the areas where management had taken place. Since other non-culled badger populations in Northern Ireland and Britain exhibited stable population trends, we attribute the reduction in relative abundance to the culling regime. Further studies of the dynamics of this reduction are required to quantify how it is counteracted by immigration from populations outside of culled areas.     

Eliminating bovine tuberculosis in cattle and badgers: insight from a dynamic model

Bovine tuberculosis (BTB) is a multi-species infection that commonly affects cattle and badgers in Great Britain. Despite years of study, the impact of badgers on BTB incidence in cattle is poorly understood. Using a two-host transmission model of BTB in cattle and badgers, we find that published data and parameter estimates are most consistent with a system at the threshold of control. The most consistent explanation for data obtained from cattle and badger populations includes within-host reproduction numbers close to 1 and between-host reproduction numbers of approximately 0.05. In terms of controlling infection in cattle, reducing cattle-to-cattle transmission is essential. In some regions, even large reductions in badger prevalence can have a modest impact on cattle infection and a multi-stranded approach is necessary that also targets badger-to-cattle transmission directly. The new perspective highlighted by this two-host approach provides insight into the control of BTB in Great Britain.